Scrota1 melanins in bats (Chiroptera): description, distribution and function

Several species of bats contain pigment granules within the scrotal skin, tunica vaginalis, or tunica albuginea surrounding the testis and/or epididymis. Seventy-two species of bats, representing 49 genera were examined for the presence of such pigmentation. Histological, chemical and spectrophotometric tests were performed and confirmed the pigment as melanin. Melanin was found only in the families Pteropidae, Megadermatidae, Myzopodidae and Vespertilionidae. A strong correlation exists between scrotal pigmentation and roosting in locations where the bats are exposed to solar radiation. Melanin pigmentation in the scrotal region appears to be an adaption protecting male germinal tissue from the harmful effects of ultraviolet radiation. In one species, Laoiu frons , melanin deposited within the scrotal skin appears to have a social/reproductive communication function.     

6种蝙蝠精子储存现象的组织学观察

精子储存是蝙蝠的生殖对策之一,有些种类的蝙蝠能将成熟精子在交配前(雄性)或交配后(雌性)储存在附睾或者输卵管及子宫内数月。采用冰冻切片和苏木精-伊红(H.E)染色法,观察了6种蝙蝠的睾丸、附睾、卵巢、输卵管和子宫,发现5种蝙蝠有精子储存现象。另外,本文还讨论了不同生殖对策蝙蝠的地理分布。     

Sexual selection drives the coevolution of male and female reproductive traits in Peromyscus mice

When females mate with multiple partners within a single reproductive cycle, sperm from rival males may compete for fertilization of a limited number of ova, and females may bias the fertilization of their ova by particular sperm. Over evolutionary timescales, these two forms of selection shape both male and female reproductive physiology when females mate multiply, yet in monogamous systems, post-copulatory sexual selection is weak or absent. Here, we examine how divergent mating strategies within a genus of closely related mice, Peromyscus, have shaped the evolution of reproductive traits. We show that in promiscuous species, males exhibit traits associated with increased sperm production and sperm swimming performance, and females exhibit traits that are predicted to limit sperm access to their ova including increased oviduct length and a larger cumulus cell mass surrounding the ova, compared to monogamous species. Importantly, we found that across species, oviduct length and cumulus cell density are significantly correlated with sperm velocity, but not sperm count or relative testes size, suggesting that these female traits may have coevolved with increased sperm quality rather than quantity. Taken together, our results highlight how male and female traits evolve in concert and respond to changes in the level of post-copulatory sexual selection.     

The frequency of multiple paternity predicts variation in testes size among island populations of house mice

Polyandry generates selection on males through sperm competition, which has broad implications for the evolution of ejaculates and male reproductive anatomy. Comparative analyses across species and competitive mating trials within species have suggested that sperm competition can influence the evolution of testes size, sperm production and sperm form and function. Surprisingly, the intraspecific approach of comparing among population variation for investigating the selective potential of sperm competition has rarely been explored. We sampled seven island populations of house mice and determined the frequency of multiple paternity within each population. Applying the frequency of multiple paternity as an index of the risk of sperm competition, we looked for selective responses in male reproductive traits. We found that the risk of sperm competition predicted testes size across the seven island populations of house mice. However, variation in sperm traits was not explained by sperm competition risk. We discuss these findings in relation to sperm competition theory, and other intrinsic and extrinsic factors that might influence ejaculate quality.     

The evolution of sperm length in moths

Sperm form and function remain poorly understood despite being of fundamental biological importance. An instructive approach has been to examine evolutionary associations across comparable taxa between sperm characters and other, potentially selective reproductive traits. We adopt this approach here in a comparative study examining how sperm lengths are associated with male and female reproductive characters across moths. Primary data have revealed Lepidoptera to be an ideal order for examination: there is profound variation in the dimensions (but not organization) of the reproductive traits between closely related species which all share a monophyletic ancestry, for example, eupyrene sperm length varies from 110 to 12,675 microm. Eupyrene (normal fertilizing) and apyrene (anucleate and non-fertile) sperm lengths are positively correlated across taxa and both sperm types show positive associations with mating pattern (as measured by the residual testis size). At fertilization, eupyrene sperm must migrate down the often elongated female spermathecal duct from storage to unite with the ovum. Across taxa, the elongation of this duct is associated with increased eupyrene sperm length, suggesting a positive female influence on sperm size since longer, more powerful sperm may be selected to migrate and/or compete successfully down greater ductal lengths. Apyrene sperm length is not associated with female reproductive tract dimensions. However, we found a positive relationship between the residual testis volume and spermathecal volume, suggesting coevolution between male investment in spermatogenesis and the extent of the female sperm storage capacity. Within males, there is a positive association between the two organs which form the ejaculate-containing spermatophore: the testes and the accessory gland. The 'trade-up' in investment to these components is discussed in relation to paternal investment and mating patterns.     

Testicular melanization has evolved in birds with high mtDNA mutation rates

Melanin is mainly found in the integument of animals, but it also appears in several extracutaneous tissues. The presence of melanin in testes has been anecdotally reported in all vertebrate groups, but the causes and functions of this melanin remain unknown. Similar to other extracutaneous melanins, testicular melanin may protect male germ cells from oxidative stress. Given the high respiratory activity of spermatozoa, oxidative stress generated by mitochondrial dysfunction as a consequence of mtDNA mutations directly affects sperm viability. Thus, natural selection may favour testicular melanization in males of species with high historical mutation rates in the mitochondrial genome. Here, we tested this hypothesis using information on occurrence of testicular melanization and mutation accumulation as reflected by cytochrome b mtDNA base pair substitution rates in a large set of 134 species of birds, controlling for the confounding effects of body mass, reproductive activity and phylogeny. We found that testicular melanization has evolved in species with high rates of accumulated mitochondrial mutations and propose that this is an adaptive response related to the protective capacity of melanin against oxidative stress. In support of this hypothesis, testicular melanization was more frequently observed during the breeding season of birds (i.e. when spermatogenesis is likely to occur) than during reproductive inactivity. In contrast to other extracutaneous melanins whose abundance seems to reflect skin and coat colour, we did not find a correlation between the proportion of plumage coloured by melanins and occurrence of testicular melanization. Whereas future experimental studies should test these hypotheses, our study highlights for the first time that melanization patterns in animals may evolve as a response to historical mutation rates.     

Male reproductive maturity and diapause termination in the leaf beetle Gastrophysa atrocyanea

Male reproductive potential and growth of testes are studied in the leaf beetle Gastrophysa atrocyanea Motschulsky (Coleoptera: Chrysomelidae) that is exposed to mild temperatures after imaginal ecdysis. Continuous administration of the Juvenile Hormone (JH) in artificial diet is highly effective with respect to stimulating testes growth and mating behaviour. Female reproductive diapause can be induced under standard rearing conditions, although optimum reproductive maturity of males is achieved at 15 °C. Treatment of males with a JH analogue accelerates testes development up to the stage of spermiogenesis (the bundling of spermatozoa) but does not promote the formation of cysts with mature sperm. Treatment with 20‐hydroxyecdysone has no influence on diapause termination and testes function. These results suggest that male reproductive maturation in G. atrocyanea is independent of JH, and moderate temperatures may induce an unknown factor that is responsible for the maturation of sperm cysts.     

A single functional testis and long deferent duct papillae: the peculiar male reproductive tract of the classically polyandrous, sex-role reversed Black Coucal (Centropus grillii)

In many birds, the male reproductive tract is asymmetric with the left testis being larger than the right one. Coucals (Centropodidae) represent an exception as the asymmetry is typically reversed. Here, we describe the functional morphology of the reproductive tract of the African Black Coucal (Centropus grillii), a bird species with reversed sex-roles and a classical polyandrous mating system. In this species, the left testis has been reduced to a tiny, disk-like vestige that in almost all cases examined was not visible macroscopically. The vestigial left testis apparently does not participate in sperm production but has retained a vestigial left excurrent duct system. By contrast, the right deferent duct was engorged with sperm, suggesting a sperm storage function. Both deferent ducts opened on the tip of spectacularly long, erectile deferent duct papillae into the urodaeum of the male cloaca. Behavioural observations suggest that they may function as “pseudophalli”. Testis mass represented 0.49% of body mass, less than half the size of other classical polyandrous bird species. Assuming moderate to high levels of sperm competition this represents a paradox. Heavy demands on the energy budget while caring for altricial young may have prevented males from maintaining two testes and large bilateral sperm storage devices. Reduced testis mass may be compensated for by frequent transfer of small amounts of sperm. Female Black Coucals have not evolved any corresponding cloacal specializations, but like all other birds have sperm storage tubules.     

Evidence of Late-Summer Mating Readiness and Early Sexual Maturation in Migratory Tree-Roosting Bats Found Dead at Wind Turbines

Understanding animal mating systems is an important component of their conservation, yet the precise mating times for many species of bats are unknown. The aim of this study was to better understand the details and timing of reproductive events in species of bats that die most frequently at wind turbines in North America, because such information can help inform conservation strategies. We examined the reproductive anatomy of hoary bats (Lasiurus cinereus), eastern red bats (L. borealis), and silver-haired bats (Lasionycteris noctivagans) found dead beneath industrial-scale wind turbines to learn more about when they mate. We evaluated 103 L. cinereus, 18 L. borealis, and 47 Ln. noctivagans from wind energy facilities in the United States and Canada. Histological analysis revealed that most male L. cinereus and L. borealis, as well as over half the Ln. noctivagans examined had sperm in the caudae epididymides by late August, indicating readiness to mate. Testes regression in male hoary bats coincided with enlargement of seminal vesicles and apparent growth of keratinized spines on the glans penis. Seasonality of these processes also suggests that mating could occur during August in L. cinereus. Spermatozoa were found in the uterus of an adult female hoary bat collected in September, but not in any other females. Ovaries of all females sampled had growing secondary or tertiary follicles, indicating sexual maturity even in first-year females. Lasiurus cinereus, L. borealis, and Ln. noctivagans are the only North American temperate bats in which most first-year young of both sexes are known to sexually mature in their first autumn. Our findings provide the first detailed information published on the seasonal timing of mating readiness in these species most affected by wind turbines.     

Movement of spermatozoa in the reproductive tract of adult male Spodoptera litura: daily rhythm of sperm descent and the effect of light regime on male reproduction

Sperm production and movement from the fused testes into the male reproductive tract of the common cutworm Spodoptera litura were studied in insects maintained in a 12 h:12 h light dark (LD) regime. Two types of sperm bundles, eupyrene (nucleated) and apyrene (anucleate) were present in the adult testes. Eupyrene bundles constituted about 25% of the total. Descent of spermatozoa from the testes into the upper vas deferens (UVD) first occurred about 24-30 h before adult eclosion. On entering the reproductive tract, eupyrene spermatozoa remained in bundles while apyrene bundles became dissociated before they reached the UVD. Downward movement of both eupyrene and apyrene spermatozoa within the male tract occurred in a daily rhythm. Sperm descent from the testes into the UVD occurred during the early scotophase, followed by their further descent into the seminal vesicle (SV) during the photophase. Spermatozoa remained in the SV for only a short duration, whence sperm quickly passed through the lower vas deferens into the duplex, which acted as the main sperm storage organ until mating was initiated. During mating 80% of sperm left the duplex, but mating did not influence the number of sperm bundles that subsequently descended into the duplex or the rate of their descent. There was no evidence of sperm reflux. Rearing in constant light (LL) and in constant dark (DD) reduced the number of eupyrene sperm present in the testes of adults that emerged in LL and DD compared to controls (LD), although there was no significant effect on the number of apyrene sperm in the testes. The rhythmic pattern of sperm descent was suppressed in both LL and DD regimes, and the number of sperm in the duplex was adversely affected, with a marked impact in LL reared insects. Male longevity, mating behaviour, oviposition and fertility were found to be more severely affected in LL than in DD.     

Male reproductive investment and queen mating-frequency in fungus-growing ants

Sperm number and male accessory gland compounds are often importantdeterminants of male mating success but have been little studiedin social insects. This is because mating in social insectsis often difficult to manipulate experimentally, and first evidencefor an explicit influence of accessory gland secretions on malemating success in social insects was obtained only recently.Here we perform a comparative analysis of male sexual organsacross 11 species of attine fungus-growing ants, representingboth genera with single- and multiple-queen mating. We foundthat the general morphology of the male sexual organs was verysimilar across all species, but the relative sizes of the accessoryglands and the sperm-containing accessory testes vary significantlyacross species. Small testes and large accessory glands characterizespecies with singly mated queens, whereas the opposite is foundin species with multiply mated queens. However, in the socialparasite Acromyrmex insinuator, in which queens have secondarilyreverted to single mating, males have accessory gland characteristicsreminiscent of the lower attine ants, but without having significantlyreduced their investment in sperm production. We hypothesizethat the main function of accessory gland compounds in attineants is to monopolize male paternity in similar ways as knownfrom other social insects. This would imply that the evolutionof polyandry in the terminal clade of the fungus-growing ants(the leafcutter ants) has resulted in selection for decreasedinvestment by males in accessory gland secretions and increasedinvestment in sperm number, in response to sperm competitionfor sperm storage.     

The Evolution of Large Testes: Sperm Competition or Male Mating Rate?

A positive relationship across species between the extent to which females mate with more than one male and relative testes mass has been demonstrated in a wide range of vertebrate taxa and certain insects. At least two hypotheses, which are not necessarily mutually exclusive, could account for this pattern: (1) the numerical sperm competition hypothesis, which assumes that larger testes enable the male to transfer more sperm to each female, giving the male an advantage in sperm competition and (2) the male mating rate hypothesis, which proposes that larger testes allow the male to produce a greater number of (potentially smaller) ejaculates to engage in frequent copulations with different females. Of these hypotheses, the former has won broad acceptance, while the latter has tended to be dismissed. Here, we argue that the lines of evidence commonly used to support the numerical sperm competition hypothesis in favour of the male mating rate hypothesis are not as clear cut or generally applicable as they are purported to be and that, consequently, the male mating rate hypothesis cannot be excluded with confidence on the basis of the current evidence. Furthermore, some evidence, such as the finding that ejaculate mass and/or sperm number is negatively correlated with testes mass across species in some insects and that larger testes in Drosophila can evolve in response to an increase in the number of females available for mating in the laboratory, provides support for the male mating rate hypothesis. Further work is needed to disentangle the relative effects of these selective pressures on the evolution of testes size.     

Sperm survival in the female reproductive tract in the fly Scathophaga stercoraria (L.)

While sperm competition risk favours males transferring many sperm to secure fertilizations, females of a variety of species actively reduce sperm numbers reaching their reproductive tract, e.g. by extrusion or killing. Potential benefits of spermicide to females include nutritional gains, influence over sperm storage and paternity, and the elimination of sperm bearing somatic mutations that would lower zygote fitness.We investigated changes in sperm viability after in vivo and in vitro exposure to the female tract in the polyandrous fly, Scathophaga stercoraria. Sperm viability was significantly lower in the females' spermathecae immediately after mating than in the experimental males' testes. Males also varied significantly in the proportion of live sperm found in storage in vivo. However, the exact mechanism of sperm degradation remains to be clarified. In vitro exposure to extracts of the female reproductive tract, including female accessory glands, failed to significantly lower sperm viability compared to controls. These results are consistent either with postcopulatory sperm mortality in vivo depending entirely on the male (with individual differences in sperm viability, motility or longevity) or with postcopulatory sperm mortality being subtly affected by female effects which were not detected by the in vitro experimental conditions. Importantly, we found no evidence in support of the hypothesis that female accessory glands contribute to sexual conflict via spermicide. Therefore, female muscular control remains to date the only ascertained mechanism of female influence on sperm storage in this species.     

Reproduction in male Pipistrellus pipistrellus (Mammalia: Chiroptera)

The annual reproductive cycle has been investigated in the male pipistrelle bat Pipistrellus pipistrellus. Spermatogenesis occurs during summer and spermatozoa are produced in August and September. The seminiferous tubules then regress rapidly but sperm are stored throughout winter in the cauda epididymidis. Little change is apparent in the morphology of the Leydig cells throughout the year, and histochemical studies have revealed no seasonal differences in the occurrence of enzymes involved in steroidogenesis. The percentage yields of testosterone and androstenedione after incubation of testis and adrenal tissues in vitro with tritiated pregnenolone have been determined and measurements made of the concentration of these hormones in testes and whole blood. Although the highest levels of these androgens are synchronous with spermatogenesis, both continue to be produced by the testes during winter. Studies in castrated bats have confirmed these observations and indicate that the activity of the accessory reproductive organs during winter is dependent on testicular androgens. The testicular cycle of the pipistrelle is not thought to be complicated by adrenal androgenesis, or storage of androgens in the brown fat. The interrelationships between reproduction and hibernation in bats are discussed.     

Microsporidia-insect host interactions: teratoid sporogony at the sites of host tissue melanization

Microsporidia Paranosema locustae and Paranosema grylli infect fat bodies of orthopteran hosts Locusta migratoria and Gryllus bimaculatus, respectively, and cause formation of nodules consisting of deposits of melanin around heavily infected cells. Both species sporadically produce enlarged or malformed (teratoid) spores as a result of abnormal sporogony. Proportions of teratospores within melanized nodules were 6-10 times higher than in surrounding non-melanized tissues. The increased numbers of teratoid microsporidian spores within melanized regions may indicate the deteriorating effect of melanin metabolites on spore morphogenesis.     

Tyrosine phosphorylation as evidence of epididymal cauda participation in the sperm maturation process of Corynorhinus mexicanus bat

The bat Corynorhinus mexicanus provides an interesting experimental model for the study of epididymal sperm maturation because after spermatogenesis and the regression of the testes, this bat stores sperm in the epididymal cauda for several months. Earlier research conducted by our group suggested that sperm maturation in this species must be completed in the caudal region of the epididymis. One of the major signal transduction events during sperm maturation is the tyrosine phosphorylation of sperm proteins. The aim of the present study was to comparatively evaluate tyrosine phosphorylation in spermatozoa obtained from the caput, corpus and cauda of the epididymis during the sperm storage period. The maturation status of the sperm was determined by the percentage of capacitation and tyrosine phosphorylation in sperm obtained from the epididymis. The highest proportion of tyrosine phosphorylation was registered after the sperm had reached the cauda epididymis during the middle of the storage period. In conclusion, in Corynorhinus mexicanus and most likely in other chiropteran species with an asynchronous male reproductive pattern, epididymal sperm maturation ends in the caudal region of the epididymis and is related to the time that the sperm remains in the epididymis before mating activity.     

Male reproductive allocation in fireflies (Photinus spp.)

Abstract. Resource allocation between somatic and reproductive structures has important fitness consequences for individuals, and optimal trade-offs are expected to depend not only on mating system differences among species but also on levels of resource stress within species. We tested the prediction that polyandry (associated with increased sperm competition) will increase male reproductive allocation in bioluminescent fireflies in Photinus spp. by comparing the relative mass of testes, seminal vesicles, and reproductive accessory glands among a monandrous and several polyandrous species. In addition, we examined a single population of a polyandrous species, Photinus greeni , to see how reproductive allocation might shift between years in response to different levels of larval resource stress. As predicted, males of P. collustrans , a monandrous species, showed a fivefold lower allocation to sperm production and a 100-fold lower allocation to reproductive accessory glands compared with males from polyandrous species. We also found evidence within P. greeni of a trade-off between allocation either to reproduction or to somatic tissue; following larval resource stress, males eclosed at significantly shorter body lengths, yet showed a 35% increase in their reproductive allocation. These results demonstrate that mating systems strongly influence male allocation to reproductive accessory glands as well as to sperm production. Furthermore, these results suggest that under larval resource stress males of Photinus spp. increase their allocation to reproduction at the expense of somatic tissue, thus maximizing their ability to produce nuptial gifts required for reproductive success.     

Morphology of male reproductive system in three species of Trypoxylon (Trypargilum) Richards (Hymenoptera: Crabronidae)

Variations in the adult male reproductive system among different groups of Hymenoptera offer characteristics that help studies on behavior and phylogenetics. The objective of this study was to describe the adult male reproductive system of three Trypoxylon (Trypargilum) species. For that, tissues were disseced, fixed in 2.5% glutaraldehyde in 0.1 M sodium cacodylate buffer, pH 7.2 and postfixed in 1% osmium tetroxide. The material was dehydratated and embedded for light and electron transmission microscopes. The species have similar reproductive systems, which are formed by a pair of testes, each one with three fusiforme follicles, from which emerges an efferent duct that later joins forming a deferent duct. The deferent duct opens into an ejaculatory duct. The first half of the deferent duct is enlarged and differentiated in a region specialized in sperm storage, the seminal vesicle. The accessory gland flows in the post-vesicular region of the deferent duct. The testes and vesicles are both covered with a conjunctive capsule. Sexually mature individuals have all spermatogenesis stages in their follicles. Sperms are released from testes in bundles which are disorganized inside seminal vesicles.     

Variation in male body size and reproductive allocation in the leafcutter ant <Emphasis Type="Italic">Atta colombica</Emphasis>: estimating variance components and possible trade-offs

Remarkably little is known about the traits that determine reproductive success of males in eusocial insects. Their window for mate choice decisions is very short, the actual mating process is very difficult to observe, and their small body sizes have likely prevented systematic studies in many species. In 2008 and 2009, we revisited a Panamanian population of Atta colombica leafcutter ants to partially repeat and complement a study of more than 15 years ago. We compared within- and between-colony variation in male body size (mass and width of head, mesosoma and gaster) and sperm characteristics (length, number and survival after exposure to saline buffer with and without added accessory gland secretion). We also measured the size of accessory glands as the main contributor of seminal fluid and the accessory testes containing all mature sperm, but we found few correlations between these variables. We also obtained little or no evidence for expected trade-offs between sperm number and sperm length and between mesosoma mass and sperm complement, although this could be due to limited sample size and unknown variation in larval resource allocation that was beyond our control. However, we found an interestingly bimodal distribution in broad-sense heritabilities (intra-class correlations) among the variables that we measured. Low heritabilities suggest that mesosoma size (mass and width), accessory testes size, sperm viability (measured as % survival in saline) and probably also accessory gland size are traits directly correlated with reproductive success. However, the much higher heritabilities for total body mass, gaster mass, head width, sperm length and sperm number suggest that these traits are less likely to make direct contributions to male fitness.     

Ejaculate production schedule and the degree of protandry in fishflies (Megaloptera: Corydalidae)

1. To examine the relationship between male–female emergence patterns and ejaculate dynamics, patterns producing sperm and seminal fluids in male internal reproductive organs, the size of a spermatophore transferred at mating and the fate of spermatophore contents moved into female storage organs were compared among the fishflies (Megaloptera: Corydalidae: Chauliodinae), Parachauliodes continentalis, P. japonicus and Neochauliodes sinensis .
2. Spermatophore contents moved into female storage organs decreased rapidly in P. japonicus and N. sinensis , but hardly at all in P. continentalis . This suggests that the females of the former two species may remate sooner than the latter species as it is known in insects that material remaining in the storage organs mechanically inhibits receptivity to mating.
3. Male P. japonicus and N. sinensis increased in internal reproductive organ mass continuously after adult eclosion, and the spermatophore size produced at the first mating increased with male age. In contrast, the internal reproductive organs of P. continentalis were relatively small and did not increase in mass after emergence. P. continentalis transferred a constantly smaller spermatophore at any copulation than the former two species.
4. Males of P. japonicus and N. sinensis emerged earlier than females, while P. continentalis showed a nearly simultaneous emergence pattern between the sexes. It seems that males of P. japonicus and N. sinensis (more polyandrous than P. continentalis ) inhibit female receptivity for a longer time period by emerging earlier and transferring larger ejaculates. In these two species, the number of sperm ejaculated at the first mating also increased with male age. The increase in sperm number by emerging earlier may be adaptive for the males owing to numerical sperm competition when the female remates.